Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant

Kelsey J. Yamada, Tolga Barker, Kimberly D. Dyer, Tyler A. Rice, Caroline M. Percopo, Katia E. Garcia-Crespo, Soochin Cho, James J. Lee, Kirk M. Druey, Helene F. Rosenberg

Research output: Contribution to journalArticle

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Abstract

RNase A is the prototype of an extensive family of divergent proteins whose members share a unique disulfide-bonded tertiary structure, conserved catalytic motifs, and the ability to hydrolyze polymeric RNA. Several members of this family maintain independent roles as ribonucleases and modulators of innate immunity. Here we characterize mouse eosinophil-associated RNase (Ear) 11, a divergent member of the eosinophil ribonuclease cluster, and the only known RNase A ribonuclease expressed specifically in response to Th2 cytokine stimulation. Mouse Ear 11 is differentially expressed in somatic tissues at baseline (brain 蠐 liver < lung < spleen); systemic stimulation with IL-33 results in 10-5000-fold increased expression in lung and spleen, respectively. Ear 11 is also expressed in response to protective priming of the respiratory mucosa with Lactobacillus plantarum; transcripts are detected both locally in lung as well as systemically in bone marrow and spleen. Mouse Ear 11 is enzymatically active, although substantially less so than mEar 1 and mEar 2; the relative catalytic efficiency (k<inf>cat</inf>/K<inf>m</inf>) of mEar 11 is diminished ∼1000-1500-fold. However, in contrast to RNase 2/EDN and mEar 2, which have been characterized as selective chemoattractants for CD11c<sup>+</sup> dendritic cells, mEar 11 has prominent chemoattractant activity for F4/80<sup>+</sup>CD11c<sup>-</sup> tissue macrophages. Chemoattractant activity is not dependent on full enzymatic activity, and requires no interaction with the pattern recognition receptor, Toll-like receptor 2 (TLR2). Taken together, this work characterizes a divergent RNase A ribonuclease with a unique expression pattern and function, and highlights the versatility of this family in promoting innate immunity.

Original languageEnglish (US)
Pages (from-to)8863-8875
Number of pages13
JournalJournal of Biological Chemistry
Volume290
Issue number14
DOIs
StatePublished - Apr 3 2015

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Eosinophil Cationic Protein
Macrophages
Chemotactic Factors
Ribonucleases
Pancreatic Ribonuclease
Eosinophils
Innate Immunity
Tissue
Pattern Recognition Receptors
Toll-Like Receptor 2
Aptitude
Disulfides
Liver
Dendritic Cells
Modulators
Brain
Cats
RNA
Cytokines

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Yamada, K. J., Barker, T., Dyer, K. D., Rice, T. A., Percopo, C. M., Garcia-Crespo, K. E., ... Rosenberg, H. F. (2015). Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant. Journal of Biological Chemistry, 290(14), 8863-8875. https://doi.org/10.1074/jbc.M114.626648

Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant. / Yamada, Kelsey J.; Barker, Tolga; Dyer, Kimberly D.; Rice, Tyler A.; Percopo, Caroline M.; Garcia-Crespo, Katia E.; Cho, Soochin; Lee, James J.; Druey, Kirk M.; Rosenberg, Helene F.

In: Journal of Biological Chemistry, Vol. 290, No. 14, 03.04.2015, p. 8863-8875.

Research output: Contribution to journalArticle

Yamada, KJ, Barker, T, Dyer, KD, Rice, TA, Percopo, CM, Garcia-Crespo, KE, Cho, S, Lee, JJ, Druey, KM & Rosenberg, HF 2015, 'Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant', Journal of Biological Chemistry, vol. 290, no. 14, pp. 8863-8875. https://doi.org/10.1074/jbc.M114.626648
Yamada KJ, Barker T, Dyer KD, Rice TA, Percopo CM, Garcia-Crespo KE et al. Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant. Journal of Biological Chemistry. 2015 Apr 3;290(14):8863-8875. https://doi.org/10.1074/jbc.M114.626648
Yamada, Kelsey J. ; Barker, Tolga ; Dyer, Kimberly D. ; Rice, Tyler A. ; Percopo, Caroline M. ; Garcia-Crespo, Katia E. ; Cho, Soochin ; Lee, James J. ; Druey, Kirk M. ; Rosenberg, Helene F. / Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant. In: Journal of Biological Chemistry. 2015 ; Vol. 290, No. 14. pp. 8863-8875.
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AU - Yamada, Kelsey J.

AU - Barker, Tolga

AU - Dyer, Kimberly D.

AU - Rice, Tyler A.

AU - Percopo, Caroline M.

AU - Garcia-Crespo, Katia E.

AU - Cho, Soochin

AU - Lee, James J.

AU - Druey, Kirk M.

AU - Rosenberg, Helene F.

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N2 - RNase A is the prototype of an extensive family of divergent proteins whose members share a unique disulfide-bonded tertiary structure, conserved catalytic motifs, and the ability to hydrolyze polymeric RNA. Several members of this family maintain independent roles as ribonucleases and modulators of innate immunity. Here we characterize mouse eosinophil-associated RNase (Ear) 11, a divergent member of the eosinophil ribonuclease cluster, and the only known RNase A ribonuclease expressed specifically in response to Th2 cytokine stimulation. Mouse Ear 11 is differentially expressed in somatic tissues at baseline (brain 蠐 liver < lung < spleen); systemic stimulation with IL-33 results in 10-5000-fold increased expression in lung and spleen, respectively. Ear 11 is also expressed in response to protective priming of the respiratory mucosa with Lactobacillus plantarum; transcripts are detected both locally in lung as well as systemically in bone marrow and spleen. Mouse Ear 11 is enzymatically active, although substantially less so than mEar 1 and mEar 2; the relative catalytic efficiency (kcat/Km) of mEar 11 is diminished ∼1000-1500-fold. However, in contrast to RNase 2/EDN and mEar 2, which have been characterized as selective chemoattractants for CD11c+ dendritic cells, mEar 11 has prominent chemoattractant activity for F4/80+CD11c- tissue macrophages. Chemoattractant activity is not dependent on full enzymatic activity, and requires no interaction with the pattern recognition receptor, Toll-like receptor 2 (TLR2). Taken together, this work characterizes a divergent RNase A ribonuclease with a unique expression pattern and function, and highlights the versatility of this family in promoting innate immunity.

AB - RNase A is the prototype of an extensive family of divergent proteins whose members share a unique disulfide-bonded tertiary structure, conserved catalytic motifs, and the ability to hydrolyze polymeric RNA. Several members of this family maintain independent roles as ribonucleases and modulators of innate immunity. Here we characterize mouse eosinophil-associated RNase (Ear) 11, a divergent member of the eosinophil ribonuclease cluster, and the only known RNase A ribonuclease expressed specifically in response to Th2 cytokine stimulation. Mouse Ear 11 is differentially expressed in somatic tissues at baseline (brain 蠐 liver < lung < spleen); systemic stimulation with IL-33 results in 10-5000-fold increased expression in lung and spleen, respectively. Ear 11 is also expressed in response to protective priming of the respiratory mucosa with Lactobacillus plantarum; transcripts are detected both locally in lung as well as systemically in bone marrow and spleen. Mouse Ear 11 is enzymatically active, although substantially less so than mEar 1 and mEar 2; the relative catalytic efficiency (kcat/Km) of mEar 11 is diminished ∼1000-1500-fold. However, in contrast to RNase 2/EDN and mEar 2, which have been characterized as selective chemoattractants for CD11c+ dendritic cells, mEar 11 has prominent chemoattractant activity for F4/80+CD11c- tissue macrophages. Chemoattractant activity is not dependent on full enzymatic activity, and requires no interaction with the pattern recognition receptor, Toll-like receptor 2 (TLR2). Taken together, this work characterizes a divergent RNase A ribonuclease with a unique expression pattern and function, and highlights the versatility of this family in promoting innate immunity.

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